Genotoxicity studies of organically grown broccoli (Brassica oleracea var. italica) and its interactions with urethane, methyl methanesulfonate and 4-nitroquinoline-1-oxide genotoxicity in the wing spot test of Drosophila melanogaster

Food and Chemical Toxicology

Volumn 48, Issue 1, 2010, Pages 120-128

  Heres Pulido, María Eugenia ^a   Dueñas García, Irma ^a   Castañeda Partida, Laura ^a   Santos Cruz, Luis Felipe ^a   Vega Contreras, Viridiana ^a   Rebollar Vega, Rosa ^a   Gómez Luna, Juan Carlos ^a   Durán Díaz, Ángel ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Broccoli; Ethyl carbamate; Modulation; Pesticides; SMART; Synergy; Vitamin C

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; CYTOCHROME P450; MESYLIC ACID METHYL ESTER; URETHAN;

ARTICLE; BROCCOLI; CHEMICAL INTERACTION; CONTROLLED STUDY; DIETARY INTAKE; DROSOPHILA MELANOGASTER; ENZYME INDUCTION; GENOTOXICITY; LARVA; NONHUMAN; ORGANIC FARMING; PLANT GROWTH; TOXICOKINETICS;

4-NITROQUINOLINE-1-OXIDE; ANIMALS; BRASSICA; CYTOCHROMES; DNA; DNA ADDUCTS; DROSOPHILA MELANOGASTER; FREE RADICAL SCAVENGERS; FREEZE DRYING; HEALTH FOOD; METHYL METHANESULFONATE; MUTAGENICITY TESTS; MUTAGENS; PURINES; QUINOLONES; REACTIVE OXYGEN SPECIES; ULTRAVIOLET RAYS; URETHANE; WING;

BRASSICA OLERACEA VAR. ITALICA; DROSOPHILA MELANOGASTER;

EID: 72149090387     PISSN: 02786915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fct.2009.09.027     Document Type: Article

References (76)

1. Abraham S.K. Antigenotoxicity of coffee in the Drosophila assay for somatic mutation and recombination. Mutagenesis 9 (1994) 383-386
2. Arima Y., Nishigori C., Takeuchi T., Oka S., Morimoto K., Utani A., and Miyachi Y. 4-Nitroquinoline 1-oxide forms 8-hydroxydeoxyguanosine in human fibroblasts through reactive oxygen species. Toxicol. Sci. 91 (2006) 382-392
3. Barrios D.B., Alatorre R.R., Bautista M.N., and Calyecac C.G. Identificación y fluctuación poblacional de plagas de col (Brassica oleracea var. capitata) y sus enemigos naturales en Acatzingo. Puebla. Agrociencia 38 (2004) 239-248
4. Barth M.M., Kerbel E.L., Broussard S., and Schmidt S.J. Modified atmosphere packaging protects market quality in broccoli spears under ambient temperature storage. J. Food Sci. 58 (2006) 1070-1072
5. Bartsch H., and Nair J. Ultrasensitive and specific detection methods for exocyclic DNA adducts: markers for lipid peroxidation and oxidative stress. Toxicology 153 (2000) 105-114
6. Brabban A.D., and Edwards C. The effects of glucosinolates and their hydrolysis products on microbial growth. J. Appl. Bacteriol. 79 (1995) 171-177
7. Cheng K.C., Cahill D.S., Kasai H., Nishimura S., and Loeb L.A. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J. Biol. Chem. 267 (1992) 166-172
8. ©. Condé Nast Digital 20 August 2008 (on line). (accessed 02.06.2009).
9. Conaway C.C., Getahun S.M., Liebes L.L., Pusateri D.J., Topham D.K., Botero-Omary M., and Chung F.L. Disposition of glucosinolates and sulforaphane in humans after ingestion of steamed and fresh broccoli. Nutr. Cancer 38 (2000) 168-178
10. Cooke M.S., Mistry N., Ahmad J., Waller H., Langford L., Bevan R.J., Evans M.D., Jones G.D., Herbert K.E., Griffiths H.R., and Lunec J. Deoxycytidine glyoxal: lesion induction and evidence of repair following vitamin C supplementation in vivo. Free Radic. Biol. Med. 34 (2003) 218-225
11. Danielson P.B., Foster J.L.M., McMahill M.M., Smith M.K., and Fogleman J.C. Induction by alkaloids and phenobarbital of family 4 cytochrome P450s in Drosophila: evidence for involvement in host plant utilization. Mol. Gen. Genet. 259 (1998) 54-59
12. Dueñas-García I.E., Vega-Contreras V., Gómez-Luna J.C., Santos-Cruz L.F., Castañeda-Partida L., Durán-Díaz A., and Heres-Pulido M.E. Toxicity parameters of 4-nitroquinoline-1-oxide, urethane and methyl methanesulfonate in the flare and Oregon-flare strains of Drosophila. Dros. Inf. Serv. 88 (2005) 83-89
13. Dunkov B.C., Guzov V.M., Mocelin G., Shotkoski F., Brun A., Amichot M., Ffrench-Constant R.H., and Feyereisen R. The Drosophila cytochrome P450 gene Cyp6a2: structure, localization, heterologous expression and induction by phenobarbital. DNA Cell Biol. 16 (1997) 1345-1356
14. Dusenbery R.L., and Smith P.D. Cellular responses to DNA damage in Drosophila melanogaster. Mutat. Res. 364 (1996) 133-145
15. El-Hamss R., Idaomar M., Alonso-Moraga A., and Muñoz-Serrano A. Antimutagenic properties of bell and black peppers. Food Chem. Toxicol. 41 (2003) 41-47
16. Fann Y.C., Metosh-Dickey C.A., Winston G.W., Sygula A., Ramakrishna R., Kadiiska M.B., and Mason R.P. Enzymatic and nonenzymatic production of free radicals from the carcinogens 4-nitroquinoline N-oxide and 4-hydroxylaminoquinoline N-oxide. Chem. Res. Toxicol. 12 (1999) 450-458
17. Franke S.I., PrÁ D., Erdtmann B., Henriques J.A., and da Silva J. Influence of orange juice over the genotoxicity induced by alkylating agents: an in vivo analysis. Mutagenesis 20 (2005) 279-283
18. 4 in mouse blood cells in vivo. Mutat. Res. 583 (2005) 75-84
19. Frei H., and Würgler F.E. Statistical methods to decide whether mutagenicity test data from Drosophila assays indicate a positive, negative, or inconclusive result. Mutat. Res. 203 (1988) 297-308
20. Frei H., and Würgler F.E. Optimal experimental design and sample size for the statistical evaluation of data from somatic mutation and recombination tests (SMART) in Drosophila. Mutat. Res. 334 (1995) 247-258
21. Frei H., Clements J., Howe D., and Würgler F.E. The genotoxicity of the anti-cancer drug mitoxantrone in somatic and germ cells of Drosophila melanogaster. Mutat. Res. 279 (1992) 21-33
22. Frölich A., and Würgler F.E. Genotoxicity of ethyl carbamate in the Drosophila wing spot test: dependence on genotype-controlled metabolic capacity. Mutat. Res. 244 (1990) 201-208
23. Fundacion Guanajuato Produce, AC, 2003. ITESM, Querétaro, México, May 2003 (on line). . (accessed 22.05.2009)
24. Gingras D., Gendron M., Boivin D., Moghrabi A., Theoret Y., and Beliveau R. Induction of medulloblastoma cell apoptosis by sulforaphane, a dietary anticarcinogen from Brassica vegetables. Cancer Lett. 203 (2004) 35-43
25. Graf U., and Singer D. Genotoxicity testing of promutagens in the wing somatic mutation and recombination test in Drosophila melanogaster. Rev. Int. Contam. Ambient. 8 (1992) 15-27
26. Graf U., and van Schaik N. Improved high bioactivation cross for the wing somatic mutation and recombination test in Drosophila melanogaster. Mutat. Res. 271 (1992) 59-67
27. Graf U., Würgler F.E., Katz A.J., Frei H., Juon H., Hall C.B., and Kale P.G. Somatic mutation and recombination test in Drosophila melanogaster. Environ. Mutagen. 6 (1984) 153-188
28. Graf U., Frei H., Kägi A., Katz A.J., and Würgler F.E. Thirty compounds tested in the Drosophila wing spot test. Mutat. Res. 222 (1989) 359-373
29. Guengerich F.P., Kim D.H., and Iwasaki M. Role of human cytochrome P-450 IIE1 in the oxidation of many low molecular weight cancer suspects. Chem. Res. Toxicol. 4 (1991) 168-179
30. Guide of Pesticides, 2007. SNSICA (Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria) Dirección General de Inocuidad Agroalimentaria, Acuícola y Pesquera, Mexico, July 2007, pp. 25-37 (on line). (accessed 22.05.2009).
31. Hällström I., Blanck A., and Atuma S. Genetic variation in cytochrome P450 and xenobiotic metabolism in Drosophila melanogaster. Biochem. Pharmacol. 33 (1984) 13-20
32. Han H., Pan Q., Zhang B., Li J., Deng X., Lian Z., and Li N. 4-NQO induces apoptosis via p53-dependent mitochondrial signaling pathway. Toxicology 230 (2007) 151-163
33. Hayes J.D., Kelleher M.O., and Eggleston I.M. The cancer chemopreventive actions of phytochemicals derived from glucosinolates. Eur. J. Nutr. 47 (2008) 73-88
34. Heres-Pulido M.E., Dueñas-García I., Castañeda-Partida L., Sánchez-García A., Contreras-Sousa M., Durán-Díaz A., and Graf U. Genotoxicity of tamoxifen citrate and 4-nitroquinoline-1-oxide in the wing spot test of Drosophila melanogaster. Mutagenesis 19 (2004) 187-193
35. Hreljac I., Zajc I., Lah T., and Filipic M. Effects of model organophosphorous pesticides on DNA damage and proliferation of HepG2 cells. Environ. Mol. Mutagen. 49 (2008) 360-367
36. Idaomar M., El-Hamss R., Bakkali F., Mezzoug N., Zhiri A., Baudoux D., Muñoz-Serrano A., Liemans V., and Alonso-Moraga A. Genotoxicity and antigenotoxicity of some essential oils evaluated by wing spot test of Drosophila melanogaster. Mutat. Res. 513 (2002) 61-68
37. Jeffery E. Component interactions for efficacy of functional foods. J. Nutr. 135 (2005) 1223-1225
38. Jeffery E.H., and Keck A.S. Translating knowledge generated by epidemiological and in vitro studies into dietary cancer prevention. Mol. Nutr. Food Res. 52 (2008) S7-S17
39. Jenkins G.J., Doak S.H., Johnson G.E., Quick E., Waters E.M., and Parry J.M. Do dose-response thresholds exist for genotoxic alkylating agents?. Mutagenesis 20 (2005) 389-398
40. Juge N., Mithen R.F., and Traka M. Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol. Life Sci. 64 (2007) 1105-1127
41. Kassie F., and Knasmuller S. Genotoxic effects of allyl isotiocyanate (AITC) and phenethyl isothiocyanate (PEITC). Chem. Biol. Interact. 127 (2000) 163-180
42. Kaya B., Creus A., Velázquez A., Yanikoǧlu A., and Marcos R. Genotoxicity is modulated by ascorbic acid. Studies using the wing spot test in Drosophila. Mutat. Res. 520 (2002) 93-101
43. Kemper R., Myers S., and Hurst H. Detoxification of vinyl carbamate epoxide by glutathione: evidence for participation of glutathione S-transferases in metabolism of ethyl carbamate. Toxicol. Appl. Pharmacol. 135 (1995) 110-118
44. Kensler T.W. Chemoprevention by inducers of carcinogen detoxification enzymes. Environ. Health Perspect. 105 (1997) 965-970
45. Kohda K., Kawazoe Y., Minoura Y., and Tada M. Separation and identification of N4-(guanosin-7-yl)-4-aminoquinoline 1-oxide, a novel nucleic acid adduct of carcinogen 4-nitroquinoline 1-oxide. Carcinogenesis 12 (1991) 1523-1525
46. Lunec J., Holloway K.A., Cooke M.S., Faux S., Griffiths H.R., and Evans M.D. Urinary 8-oxo-2′-deoxyguanosine: redox regulation of DNA repair in vivo?. Free Radical. Biol. Med. 33 (2002) 875-885
47. McCarty M.F. Inhibition of CYP2E1 with natural agents may be a feasible strategy for minimizing the hepatotoxicity of ethanol. Med. Hypotheses 56 (2001) 8-11
48. Mirzayans R., Bashir S., Murray D., and Paterson M.C. Inverse correlation between p53 protein levels and DNA repair efficiency in human fibroblast strains treated with 4-nitroquinoline 1-oxide: evidence that lesions other than DNA strand breaks trigger the p53 response. Carcinogenesis 20 (1999) 941-946
49. Morris C.R., Chen S.C., Zhou L., Schopfer L.M., Ding X., and Mirvish S.S. Inhibition by allyl sulfides and phenethyl isothiocyanate of methyl-n-pentylnitrosamine depentylation by rat esophageal microsomes, human and rat CYP2E1, and rat CYP2A3. Nutr. Cancer 48 (2004) 54-63
50. Musk S.R., Smith T.K., and Johnson I.T. On the cytotoxicity and genotoxicity of allyl and phenethyl isothiocyanates and their parent glucosinolates sinigrin and gluconasturtiin. Mutat. Res. 348 (1995) 19-23
51. Nagao M., and Sugimura T. Molecular biology of the carcinogen, 4-nitroquinoline 1-oxide. Adv. Cancer Res. 23 (1976) 131-169
52. Nakahara W., Fukuoka F., and Sugimura T. Carcinogenic action of 4-nitroquinoline-N-oxide. Gann 48 (1957) 129-137
53. Nivard M.J.M., Pastink A., and Vogel E.W. Molecular analysis of mutations induced in the vermilion gene of Drosophila melanogaster by methyl methanesulfonate. Genetics 131 (1992) 673-682
54. NutritionData.com, 2009. Condé Nast Digital (on line). (accessed 20.02.2009).
55. Oregon Tilth Certified Organic (OTCO), 2009 (on line). (accessed 20.02.2009).
56. Paolini M., Perocco P., Canistro D., Valgimigli L., Pedulli G.F., Iori R., Croce C.D., Cantelli-Forti G., Legator M.S., and Abdel-Rahman S.Z. Induction of cytochrome P450, generation of oxidative stress and in vitro cell-transforming and DNA-damaging activities by glucoraphanin, the bioprecursor of the chemopreventive agent sulforaphane found in broccoli. Carcinogenesis 25 (2004) 61-67
57. Pérez M.A., Segura A., García R., Colinas T., Pérez M., Vázquez A., and Navarro H. Residuos de plaguicidas organofosforados en cabezuela de brócoli (Brassica oleracea) determinados por cromatografía de gases. Rev. Int. Contam. Ambient. 25 (2009) 103-110
58. Petri N., Tannergren C., Holst B., Mellon F.A., Bao Y., Plumb G.W., Bacon J., O'Leary K.A., Kroon P.A., Knutson L., Forsell P., Eriksson T., Lennernas H., and Williamson G. Absorption/metabolism of sulforaphane and quercetin, and regulation of phase II, in human jejunum in vivo. Drug Metab. Dispos. 31 (2003) 805-813
59. Podse{ogonek}dek A. Natural antioxidants and antioxidant capacity of Brassica vegetables: a review. LWT Food Sci. Technol. 40 (2007) 1-11
60. Robbins R.J., Keck A.S., Banuelos G., and Finley J.W. Cultivation conditions and selenium fertilization alter the phenolic profile, glucosinolate, and sulforaphane content of broccoli. J. Med. Food 8 (2005) 204-214
61. Rodriguez-Arnaiz R., Soto P.O., Oyarzún J.C., and Graf U. Analysis of mitotic recombination induced by several mono- and bifunctional alkylating agents in the Drosophila wing-spot test. Mutat. Res. 351 (1996) 133-145
62. Rouzaud G., Rabot S., Ratcliffe B., and Duncan A.J. Influence of plant and bacterial myrosinase activity on the metabolic fate of glucosinolates in gnotobiotic rats. Br. J. Nutr. 90 (2003) 395-405
63. Rowe L.A., Degtyareva N., Paul W., and Doetsch P.W. DNA damage-induced reactive oxygen species (ROS) stress response in Saccharomyces cerevisiae. Free Radical. Biol. Med. 45 (2008) 1167-1177
64. Rungapamestry V., Duncan A.J., Fuller Z., and Ratcliffe B. Influence of blanching and freezing broccoli (Brassica oleracea var. italica) prior to storage and cooking on glucosinolate concentrations and myrosinase activity. Eur. Food Res. Technol. 227 (2008) 37-44
65. Salazar-Arredondo E., de Jesús Solís-Heredia M., Rojas-García E., Hernández-Ochoa I., and Quintanilla-Vega B. Sperm chromatin alteration and DNA damage by methyl-parathion, chlorpyrifos and diazinon and their oxon metabolites in human spermatozoa. Reprod. Toxicol. 25 (2008) 455-460
66. Salmon T.B., Evert B.A., Binwei Song B., and Doetsch P.W. Biological consequences of oxidative stress-induced DNA damage in Saccharomyces cerevisiae. Nucleic Acids Res. 32 (2004) 3712-3723
67. Saner C., Weibel B., Würgler F.E., and Sengstag C. Metabolism of promutagens catalyzed by Drosophila melanogaster CYP6A2 enzyme in Saccharomyces cerevisiae. Environ. Mol. Mutagen. 27 (1996) 46-58
68. Stephensen P.U., Bonnesen C., Schaldach C., Andersen O., Bjeldanes L.F., and Vang O. N-Methoxyindole-3-carbinol is a more efficient inducer of cytochrome P-450 1A1 in cultured cells than indol-3-carbinol. Nutr. Cancer 36 (2000) 112-121
69. Thomas J.H. Rapid birth-death evolution specific to xenobiotic cytochrome P450 genes in vertebrates. PLoS Genet. 3 (2007) e67
70. Tiku A.B., Abraham S.K., and Kale R.K. Protective effect of the cruciferous vegetable mustard leaf (Brassica campestris) against in vivo chromosomal damage and oxidative stress induced by gamma-radiation and genotoxic chemicals. Environ. Mol. Mutagen. 49 (2008) 335-342
71. Traka M., Gasper A.V., Melchini A., Bacon J.R., Needs P.W., Frost V., Chantry A., Jones A.M., Ortori C.A., Barrett D.A., Ball R.Y., Mills R.D., and Mithen R.F. Broccoli consumption interacts with GSTM1 to perturb oncogenic signaling pathways in the prostate. PLoS ONE 3 (2008) 1-14
72. Trinh K., Moore K., Wes P.D., Muchowski P.J., Dey J., Andrews L., and Pallanck L.J. Induction of the phase II detoxification pathway suppresses neuron loss in Drosophila models of Parkinson's disease. J. Neurosci. 28 (2008) 465-472
73. Verhoeven D.T., Verhagen H., Goldbohm R.A., van den Brandt P.A., and van Poppel G. A review of mechanisms underlying anticarcinogenicity by brassica vegetables. Chem. Biol. Interact. 103 (1997) 79-129
74. Yang J., McCart C., Woods D.J., Terhzaz S., Greenwood K.G., Ffrench-Constant R.H., Julian A.T., and Dow J.A.T. A Drosophila systems approach to xenobiotic metabolism. Physiol. Genomics 30 (2007) 223-231
75. Zhou C., Poulton E.J., Grün F., Bammler T.K., Blumberg B., Thummel K.E., and Eaton D.L. The dietary isothiocyanate sulforaphane is an antagonist of the human steroid and xenobiotic nuclear receptor. Mol. Pharmacol. 71 (2007) 220-229
76. Zhu C.Y., and Loft S. Effect of chemopreventive compounds from Brassica vegetables on NAD(P)H:quinone reductase and induction of DNA strand breaks in murine hepa1c1c7 cells. Food Chem. Toxicol. 41 (2003) 455-462